Professional Documents
Culture Documents
Table 1. Effectiveness of methods currently used to study the functioning of human cerebral areas
these different methods are really complementary to our posterior wall. This finding shows a high degree of
understanding of how the cerebral cortex controls a homology in the organization of the FEF in humans and
paradigm. This complementation explains the recent monkeys [5,6 .]. Furthermore, by using labelled tissue
rapid advance in our knowledge of eye movement sections in post-mortem human brains, it has been
organization, and even of the role of some neuropsycho- shown that the area defined by fMRI studies within the
logical processes in preparing the movement generally precentral sulcus may be classified by chemoarchitectur-
when, for example, saccades are used as a tool or model al criteria as a motor cortex, a result which was expected
for motricity. This review will, therefore, mainly focus on considering the FEF’s functions in PEM control and
the latest advances in our knowledge of the control of saccade triggering [7 .]. In the precentral sulcus, besides
human eye movements at the cortical level. The roles of the main locus of the FEF, located at the junction with
some areas located in the frontal lobe, the parietal lobe the superior frontal sulcus, another locus of activation is
and the cingulate cortex will be reviewed, successively, often observed in fMRI studies along the lateral part of
before a brief concluding overview of the main pathways this sulcus and the adjacent portion of the precentral
existing between them. gyrus [8,9]. The specific role of this lateral locus remains
to be determined, since it is activated both by single and
Frontal lobe combined eye and head movements [10 .].
In the frontal lobe, three main areas are involved in eye
movement control [2]: the frontal eye field (FEF), the Pursuit eye movements
supplementary eye field (SEF) and the dorsolateral Interestingly, in two electrical stimulation studies of the
prefrontal cortex (DLPFC). human FEF, contralateral slow eye deviations were
observed [11 .,12 .]. Such slow eye deviations could
The frontal eye field correspond to PEMs given their speed characteristics.
The FEF is involved in the preparation and triggering of The stimulation sites of these slow eye deviations were
all intentional saccades, which are internally triggered located in the precentral sulcus, more posterior than the
towards a target already present (intentional visually stimulation sites for saccades [12 .], a finding which is in
guided saccade), not yet present (predictive saccade), no accordance with fMRI data [4]. However, it should be
longer visible (memory-guided saccade) or located in the noted that the human cerebral hemisphere, including
opposite direction (antisaccade) [2]. This area is less the FEF, controls mainly ipsilateral PEMs, even though
involved in the triggering of reflexive visually guided experimental data [5,6 .] and human lesion studies [13]
saccades (often called ‘pro-saccades’), which are exter- suggest that some degree of contralateral control by each
nally triggered towards a suddenly appearing peripheral area also exists. To explain this apparent discrepancy
target and are mainly dependent upon the parietal eye between this mainly ipsilateral hemispheric control of
field (PEF). The FEF also controls pursuit eye move- PEMs and the results of electrical stimulation studies, it
ments (PEMs), along with the posterior parieto-temporal may be assumed that stimulation, which was superficial
areas. Recent findings on the FEF mainly concern its in the FEF region in these studies, in fact involved only
location and its role in the control of PEMs. sites controlling contralateral PEMs. Indeed, such sites
could be located, as in the monkey [14], more super-
Location ficially than the ipsilateral PEM sites [12 .]. Like lesion
Studies using fMRI have delimited the location of the studies [13], fMRI studies suggest that the FEF also
FEF mainly to the intersection between the precentral controls optokinetic nystagmus [15], with an activation
sulcus and the superior frontal sulcus (Fig. 1) [3]. Thanks existing in this area and in the other posterior hemi-
to a recent fRMI study [4], using 3-tesla, the saccade- spheric cerebral areas involved in PEM, but also with
related area of the FEF has been localized to the upper concomitant deactivation of the different cerebral areas
portion of the anterior wall of the precentral sulcus, and involved in the vestibular control [16 .]. Such results
the pursuit-related area to a deeper region along the could be due to a reciprocal inhibitory visuo-vestibular
anterior wall, the fundus and the deep part of the interaction existing at the cortical level in order to
Cerebral cortex eye movement control Pierrot-Deseilligny et al. 19
Decision: SEF
Pre-SEF Visuo-
Inhibition cs spatial
Prediction sfs post-cs
CEF attention?
Short-term
spatial memory FEF
DLPFC
pcs ips Visuo-
SPL spatial
PCC integration
SMG
ifs
SMG IPA
Visual
ls AG information
PEF ips
sts
+
AG
– pos
PHC +
HF
SC
RF Reflexive
Medium-term Long-term saccade
spatial memory? spatial memory? Execution triggering
SEF, supplementary eye field; sfs, superior frontal sulcus; CEF, cingulate eye field; cs, central sulcus; DLPFC, dorsolateral prefrontal cortex; pcs,
precentral sulcus; FEF, frontal eye field; ips, intraparietal sulcus; ifs, inferior frontal sulcus; SMG, supramarginal gyrus; PCC, posterior cingulate
cortex; SPL, superior parietal lobule; IPA, intraparietal areas; ls, lateral sulcus; AG, angular gyrus; PEF, posterior eye field; sts, superior temporal
sulcus; pos, parieto-occipital sulcus; PHC, parahippocampal cortex; HF, hippocampal formation; SC, superior colliculus; RF, reticular formations.
maintain the perception of self-motion. Finally, in the antisaccade, made in the direction opposite to the target
monkey, it has been shown that the FEF neurons by the FEF. Pro-saccades (reflexive visually guided
controlling PEMs are also involved in vergence, a result saccades) and antisaccades were studied using fMRI in
which suggests that PEMs are coded in three-dimen- two reports [18 .,19 . .]. In both reports, activation was
sional space by the frontal cortex [17 .]. observed just before antisaccades in the FEF but not in
the PEF, confirming that such intentional saccades
Saccades require an early preparation by the former but not by
Antisaccades are intentional saccades which have to be the latter. However, contrary to a suggestion existing in
made in the direction opposite to a suddenly appearing another recent fMRI study [20], this does not mean that
peripheral visual target. These saccades comprise two inhibition of misdirected reflexive pro-saccades is
different mechanisms [2]: (1) inhibition of an unwanted organized in the FEF. In fact, an activation of the right
reflexive misdirected saccade, triggered towards the DLPFC was also noted just before antisaccades in one of
visible target by the PEF when such inhibition – being these fMRI studies [19 . .], in accordance with the results
under the control of the DLPFC (see below) – is no of previous functional imaging studies [21,22]. Taken
longer efficient; the percentage of these misdirected together, these fMRI studies confirm the results of
saccades (i.e. errors) reflects the inhibition function; and lesion studies with specific damage to the DLPFC or the
(2) concomitant triggering of an intentional correct FEF that had previously clearly shown that inhibition of
20 Neuro-ophthalmology and neuro-otology
300 ms 25 s 5mn
Visuo-spatial Short-term Medium-term Long-term
integration
Timea
is controlled by the hippocampal formation [32], but responses, could be exerted through inhibitory interac-
further studies are needed to confirm this. To conclude tions between neurons in the DLPFC, controlling the
this review on the study of spatial memory using timing of neuronal activities during cognitive operations
memory-guided saccades, it should be pointed out that and thereby shaping the temporal flow of information
this is a good example of how eye movements may be [41].
studied not simply per se but also used as a tool in
neuropsychological or neuroscience research. Parietal lobe
In the parietal lobe, the location and function of the
Decision different areas involved in eye movements and attention
The DLPFC is also involved in the control of predictive are not well known.
saccades. In this paradigm, a visual target moves to
locations and at times that are entirely predictable. Anatomy
Normal subjects soon start to make predictive saccades, The parietal lobe and more particularly its posterior part,
anticipating the location to which the target is moving. the PPC, are involved in the control of saccades and
After lesions limited to the DLPFC, the percentage of attention. The PPC includes the intraparietal sulcus
predictive saccades significantly decreases [24 .]. These (IPS) extending from the post-central sulcus anteriorly to
results in conjunction with those referred to above the parieto-occipital sulcus posteriorly (Fig. 1). The IPS
suggest that the DLPFC plays a crucial role in decisional is slightly oblique along the antero-posterior axis, and so
processes governing eye movement behaviour, preparing is more lateral anteriorly and more medial posteriorly.
intentional saccades by inhibiting unwanted reflexive The IPS, which is a deep sulcus, separates the superior
saccades (inhibition), maintaining memorized informa- parietal lobule (SPL) located medially (i.e. Brodmann
tion for forthcoming intentional saccades (short-term area 7) from the inferior parietal lobule, located laterally.
spatial memorization) or facilitating intentional anticipa- The latter comprises Brodmann area 40 (i.e. the
tory saccades (prediction), depending upon current supramarginal gyrus), lying anteriorly around the ex-
external environmental and internal circumstances tremity of the lateral sulcus, and Brodmann area 39 (i.e.
[24 .]. In support of this decisional role, it may be the angular gyrus), lying posteriorly around the extremity
mentioned that in an fMRI study in normal subjects, of the superior temporal sulcus (Fig. 1). Thus, the
self-selecting the direction of the forthcoming saccade, anatomy of the IPS is not simple, being relatively
the DLPFC was strongly activated during the selection variable from one subject to another. Furthermore, in
period (Milea et al., in preparation). This decisional role, fMRI studies, it is difficult to differentiate activation
which is important in guiding or inhibiting future related to saccades from that related to attention,
22 Neuro-ophthalmology and neuro-otology
because a saccade always includes a shift of attention and tions appear to be qualitatively different, with a more
a pure shift of visual attention usually activates saccade visual involvement for the parieto-FEF projection and
areas (e.g. the FEF) [2]. Consequently, the precise a more saccadic involvement for the parieto-superior
locations within the PPC of regions specifically control- colliculus projection [62]. The parieto-FEF projection
ling saccades or attention remain relatively uncertain. could be mainly involved in visual fixation [13]. The
results of a study in patients with lesions affecting the
The parietal eye field and attentional areas posterior part of the internal capsule [63 .], damaging
The human PEF corresponds to the lateral intraparietal the direct parieto-collicular tract originating in the
area of the monkey. The lateral intraparietal area is PEF, are in accordance with experimental results and
involved in the control of saccades [42], but also in confirm that the PEF is crucial for reflexive saccade
attentional processes [43 .,44 . .]. Furthermore, light generation [23] but not for intentional saccade genera-
stimulation of this area in the monkey results in a tion. The latter depends mainly upon FEF control
simple shift of visual attention (without eye movement), (see above).
whereas stronger stimulation results in a saccade [45 .].
These results emphasize the close links existing Cingulate cortex
between saccades and attention, even in the same area. The cingulate cortex is divided into the anterior
The PEF appears to be located along the IPS [46], cingulate cortex (ACC) (Brodmann area 24) and the
within the sulcus, and, more precisely, after comparing posterior cingulate cortex (PCC) (Brodmann area 23).
the results of several more recent fMRI studies on The posterior part of the ACC is involved in saccade
saccades or visual attention [47–50,51 .,52 . .], in its control [64], more precisely in intentional saccade
posterior half, adjacent laterally to the anterior part of control, but not in reflexive saccade control [65]. This
the angular gyrus (Brodmann area 39) and medially to ‘cingulate eye field’ (CEF), located at the limit between
the posterior part of the SPL (Brodmann area 7). In this Brodmann areas 23 and 24, could, via an intentional
posterior IPS area and on the basis of the results of an motivation process, prepare all the frontal ocular motor
fMRI study, using 4-tesla, the PEF could be located areas involved in intentional saccade control to act in the
mainly in the medial wall of the IPS [53 .]. The forthcoming motor behaviour. The DLPFC is also under
activation of the PEF is also modulated by head position the control of the CEF, as suggested – after CEF lesions
[51 .], a result which is probably related to the role of this – by memory-guided saccade abnormalities [65] and by
area in visuo-spatial integration. Concerning this func- saccade inhibition impairment in the antisaccade para-
tion, a recent TMS study [54] showed that the extra- digm [66 .].
retinal signals required to determine the amplitude of
the second saccade in the double-step paradigm reach The role of the PCC is less well known, because in the
the PPC, probably via the efferent-copy pathways, only monkey this area is influenced by saccade activity, but
100 ms before the triggering of this saccade [54]. FMRI with a discharge occurring only after the saccade onset
studies [53 .,55 .] have also shown that a spatial updating [67]. An fMRI study has shown that the PCC is active
of visual information occurs in the human PPC (includ- during reflexive saccades but not during intentional
ing the PEF region) after an eye movement. saccades [60 .]. Thus, the PCC appears to be the
equivalent, for reflexive saccade control, of the CEF
There is now accumulative evidence, on the basis of (within the ACC) for intentional saccade control,
fMRI studies, to suggest that the anterior part of the IPS namely by preparing the PEF to possibly act with a
(limited medially by the supramarginal gyrus, i.e. reflexive saccade when attentional processes become
Brodmann area 40) is more involved in eye–hand predominant. The PCC is also activated during PEM
coordination [47,49,56], and the posterior part of the [68,69 .]. Therefore, from an ocular motor point of view,
SPL (close to the adjacent PEF) in attentional processes the CEF (ACC) could prepare the forthcoming
[48,49,52 . .,56,57 .]. Furthermore, the supramarginal intentional eye movements, which are internally
gyrus (Brodmann area 40), during saccades [58] or purely governed, whereas the PCC could control the other,
attention paradigms [48,49,57 .,59], and the angular gyrus externally-triggered eye movements: the reflexive
(Brodmann area 39), during reflexive saccades [60 .], saccades and smooth pursuit. PCC activity also appears
have more rarely been activated in fMRI studies. to be related to attentional processes, though its precise
However, this also suggests a control of these areas in role in this field is still unclear. Two fMRI studies,
attention. These results may be related to the well- however, have suggested that the PCC is activated in
known visual neglect syndrome due to right PPC lesions purely attentional paradigms as soon as an informative
affecting more particularly the angular gyrus [61]. cue indicates an imminent shift of visual attention
[70,71 .]. The PCC is connected to the IPS [71 .], but
The PEF projects to both the FEF and the superior further studies are needed to determine the precise
colliculus (Fig. 1). In the monkey, these two projec- role of this pathway.
Cerebral cortex eye movement control Pierrot-Deseilligny et al. 23
of these different areas in attention control remain to be 3 Paus T. Location and function of the human frontal eye field: a selective
review. Neuropsychologia 1996; 34:475–483.
determined. These areas probably interact and inter-
4 Rosano C, Krisky CM, Welling JS, et al. Pursuit and saccadic eye movement
connect with the PCC, influencing them upstream via subregions in human frontal eye field: a high-resolution fMRI investigation.
an attentional motivation process. The PEF or a closed Cereb Cortex 2002; 12:107–115.
area also controls visuo-spatial integration. A reflexive 5 Gottlieb JP, MacAvoy MG, Bruce CJ. Neural responses related to smooth-
saccade is triggered by the PEF if external circum- pursuit eye movements and their correspondence with electrically elicited
smooth eye movements in the primate eye field. J Neurophysiol 1994;
stances require such a rapid response. This triggering is 72:1634–1653.
performed via the direct parieto-collicular tract passing 6 Tanaka M, Lisberger SG. Role of arcuate frontal cortex of monkeys in smooth
through the posterior part of the internal capsule. In the . pursuit eye movements. I. Basic response properties to retinal image motion
and position. J Neurophysiol 2002; 87:2684–2699.
event of a delayed response, visual information is The site related to pursuit eye movements is anatomically and functionally separate
transmitted from the PEF to the FEF for active fixation from the saccadic frontal eye field.
and from the intraparietal areas to the DLPFC for short- 7 Rosano C, Sweeney JA, Melchitzky DS, Lewis DA. The human precentral
. sulcus: chemoarchitecture of a region corresponding to the frontal eye fields.
term spatial memorization (between 300 ms and 25 s).
Brain Res 2003; 972:16–30.
The DLPFC is involved in decisional processes This study provided evidence that the human FEF region identified in the precentral
governing ocular motor behaviour by inhibiting un- sulcus using fMRI is indeed characterized by a distinctive chemoarchitecture.
wanted reflexive saccades (inhibition) controlled by the 8 Lobel E, Kahane P, Leonards U. Localization of the human frontal eye fields:
anatomical and functional findings from fMRI and intracerebral electrical
PEF or facilitating the triggering of anticipatory saccades stimulation. J Neurosurg 2001; 95:804–815.
(prediction) by the FEF. The inhibition of reflexive
9 Gagnon D, O’Driscoll GA, Petrides M, Pike GB. The effect of spatial and
saccades originating in the DLPFC is probably exerted temporal information on saccades and neural activity in oculomotor
directly on the superior colliculus. When the response structures. Brain 2002; 125:123–139.
delays are longer, the PHC for medium-term spatial 10 Petit L, Beauchamp M. Neural basis of visually guided head movements
. studied with fMRI. J Neurophysiol 2003; 89:2516–2527.
memory (between 25 s and a few minutes) and the The role of the lateral part of the FEF, within the lateral portion of the precentral
hippocampal formation for long-term spatial memory sulcus, is discussed.
(after a few minutes) store memorized information, 11 Milea D, Lobel E, Lehéricy S, et al. Intraoperative frontal eye field stimulation
. elicits ocular deviation and saccade suppression. Neuroreport 2002;
reaching the medial temporal areas probably both
13:1359–1364.
serially from the DLPFC and in parallel from the Electrical stimulation of the frontal eye field may suppress self-paced saccades
PPC. The execution of intentional saccades is per- and elicit contralateral slow eye deviations.
formed by the FEF, which is prepared to respond by 12 Blanke O, Seeck M. Direction of saccadic and smooth eye movements
. induced by electrical stimulation of the human frontal eye field: effect of orbital
the CEF (located in the ACC) influencing, via an position. Exp Brain Res 2003; 150:174–183.
intentional motivation process, all other frontal ocular This provides an interesting discussion about the significance of contralateral slow
eye deviations elicited by electrical stimulation.
motor areas. When motor programmes, comprising either
a sequence of several successive saccades or single 13 Rivaud S, Müri RM, Gaymard B, et al. Eye movement disorders after frontal
eye field lesions in humans. Exp Brain Res 1994; 102:110–120.
saccades combined with body movements, are planned,
14 Gottlieb JP, Bruce CJ, MacAvoy MG. Smooth eye movement elicited by
this involves the SEF just before the execution, after a microstimulation in the primate frontal eye field. J Neurophysiol 1993;
probable learning in the pre-SEF. PEMs are controlled 69:786–799.
by the posterior hemispheric areas (not shown), located 15 Dieterich M, Bucher SF, Seelos KC, Brandt T. Horizontal or vertical
close to the angular gyrus at the temporo-parieto- optokinetic stimulation activates visual motion-sensitive, ocular motor and
vestibular cortex areas with right hemispheric dominance. A fMRI study. Brain
occipital junction (medial superior temporal area and 1998; 121:1479–1495.
middle temporal area), but also by the FEF, the specific 16 Dieterich M, Bense S, Stephan T, et al. FMRI signal increases and decreases
.
role of which in PEM generation is not yet really clear. in cortical areas during small-field optokinetic stimulation and central fixation.
Exp Brain Res 2003; 148:117–127.
Finally, the recent period has been rich in new These authors describe an increase in activation in areas controlling optokinetic
information and interpretations concerning the cortical nystagmus, including the FEF, with concomitant decrease in the cortical areas
involved in vestibular control, which could be related to a reciprocal visuo-
control of eye movements in humans, thanks to some vestibular inhibition existing at the cortical level for the perception of self-motion.
lesion studies and especially to TMS and fMRI studies, 17 Fukushima K, Yamanobe T, Shinmei Y, et al. Coding of smooth eye
which are currently in full development and can be . movements in three-dimensional space by the frontal cortex. Nature 2002;
419:157–162.
expected to produce significant new advances in the This reveals an important new finding on the FEF which is well summarized in the
near future. paper title.
24 Neuro-ophthalmology and neuro-otology
18 Connolly JD, Goodale MA, Menon RS, Munoz DP. Human fMRI evidence for 39 Nyffeler T, Pierrot-Deseilligny C, Felblinger J, et al. Time-dependent
. the neural correlates of preparatory set. Nat Neurosci 2002; 5:1345–1352. . hierarchical organization of spatial working memory: a transcranial magnetic
Antisaccades are prepared in the FEF, but this does not mean, according to the stimulation study. Eur J Neurosci 2002; 16:1823–1827.
authors, that this area is involved in saccade inhibition. This is an interesting contribution to the study of spatial memory in the human
dorsolateral prefrontal cortex.
19 De Souza JFX, Menon RS, Everling S. Preparatory set associated with pro-
.. saccades and anti-saccades in humans investigated with event-related fMRI. 40 Nyffeler T, Pierrot-Deseilligny C, Hess CW, Müri RM. Parallel and serial
J Neurophysiol 2003; 89:1016–1023. processing components in memory-guided saccades. Exp Brain Res 2004;
In this study, an activation of the right DLPFC and of both FEF was observed just 154:109–112.
before antisaccades, showing that these two types of frontal areas are involved in
the preparation of such saccades. 41 Constantinidis C, Williams GV, Goldman-Rakic P. A role for inhibition in
shaping the temporal flow of information in prefrontal cortex. Nat Neurosci
20 Cornelissen FW, Kimmig H, Shira M, et al. Event-related fMRI responses in 2002; 5:175–180.
the human frontal eye fields in a randomized pro- and antisaccade task. Exp
Brain Res 2002; 145:270–274. 42 Leigh RJ, Zee DS. The neurology of eye movements. 3rd ed. Oxford: Oxford
University Press; 1999.
21 Sweeney JA, Mintun MA, Kwee S, et al. Positron emission tomography study
of voluntary saccadic eye movements and spatial working memory. J 43 Wardak C, Olivier E, Duhamel JR. Saccadic target selection deficits after
. lateral intraparietal area inactivation in monkeys. J Neurosci 2002; 22:9877–
Neurophysiol 1996; 75:454–458.
9884.
22 Merriam EP, Colby CL, Thulborn KR, et al. Stimulus-response incompatibility This study on the monkey PEF showed that the area is important for selecting
activates cortex proximal to three eye fields. NeuroImage 2001; 13:794–800. visual targets.
23 Pierrot-Deseilligny C, Rivaud S, Gaymard B, Agid Y. Cortical control of 44 Bilsey JW, Goldberg ME. Neuronal activity in the lateral intraparietal area and
reflexive visually guided saccades. Brain 1991; 114:1473–1485. .. spatial attention. Science 2003; 299:81–86.
24 Pierrot-Deseilligny C, Müri RM, Ploner CJ, et al. Decisional role of the The lateral intraparietal area (PEF) is also clearly involved in attentional processes.
. dorsolateral prefrontal cortex in ocular motor behaviour. Brain 2003;
45 Cutrell EB, Marrocco RT. Electrical stimulation of primate posterior parietal
126:1460–1473. . cortex initiates orienting and alerting components of covert attention. Exp
This was the first lesion study in humans with lesions limited to the DLPFC (area
Brain Res 2002; 144:103–113.
46 of Brodmann), i.e. in the middle frontal gyrus, and report of the spectrum of
Depending upon the stimulation intensity, a simple shift of attention or a saccade is
abnormalities existing in all usual saccade paradigms, suggesting a decisional role
elicited by PPC stimulation.
of this area in ocular motor behaviour. In addition, the authors provide a useful
comparison with abnormalities observed after pure FEF lesions. 46 Müri RM, Iba-Zizen MT, Derosier C, et al. Location of the human posterior
25 Gaymard B, François C, Ploner CJ, et al. A direct prefrontotectal tract eye field with functional magnetic resonance imaging. J Neurol Neurosurg
. against distractibility in the human brain. Ann Neurol 2003; 53:542–545. Psychiatry 1996; 60:445–448.
This is a case report and anatomical study on the human prefronto-collicular 47 Kawashima R, Naitoh E, Matsumara M, et al. Topographic representation in
pathway. human intraparietal sulcus of reaching and saccade. NeuroReport 1996;
26 Tanaka H, Arai M, Kubo J, Hirata K. Conjugate eye deviation with head 7:1253–1256.
. version due to cortical infarction of the frontal eye field. Stroke 2002; 5:642– 48 Büchel C, Josephs O, Rees G, et al. The functional anatomy of attention to
643. visual motion. Brain 1998; 121:1281–1294.
A conjugate eye deviation may be observed after a small cortical infarction limited
to the frontal eye field. 49 Simon O, Mangin JF, Cohen L, et al. Topographical layout of hand, eye,
calculation and language-related areas in the human parietal lobe. Neuron
27 Grosbras MH, Lobel E, Van de Moortele PF, et al. An anatomical landmark 2002; 33:475–487.
for the supplementary eye fields in human revealed with functional magnetic
resonance imaging. Cereb Cortex 1999; 9:705–711. 50 Culham JC, Kanwisher NG. Neuroimaging of cognitive functions in human
parietal cortex. Curr Opin Neurobiol 2001; 11:157–163.
28 Luppino G, Rozzi S, Calzavara R, Matelli M. Prefrontal and agranular
. cingulate projections to the dorsal premotor areas F2 and F7 in the macaque 51 Brotchie PR, Lee MB, Chen DY, et al. Head position modulates activity in the
monkey. Eur J Neurosci 2003; 17:559–578. . human parietal eye fields. NeuroImage 2003; 18: 178-184.
This is a new contribution to the anatomical connections of the supplementary eye The human PEF is located in the posterior part of the intraparietal sulcus and its
field. activity is modulated by head position.
29 Isoda M, Tanji J. Cellular activity in the supplementary eye field during 52 Macaluso E, Driver J, Frith CD. Multimodal spatial representations engaged
. sequential performance of multiple saccades. J Neurophysiol 2002; .. in human parietal cortex during both saccadic and manual spatial orienting.
88:3541–3545. Curr Biol 2003; 13:990–999.
The SEF neurons are involved in the coding of temporally ordered saccadic eye In this interesting study, clever paradigms and a conjunction analysis suggested
movements (sequences). that the posterior part of the superior parietal lobule and the anterior part of the
30 Tobler PN, Müri RM. Role of human frontal and supplementary eye fields in intraparietal sulcus are involved in attentional processes but not in motor (saccade)
double step saccades. NeuroReport 2002; 13:253–255. execution.
31 Coe B, Tomihara K, Matsusawa M, Hikosaka O. Visual and anticipatory bias 53 Medendorp WP, Goltz HC, Vilis T, Crawford JD. Gaze-centered updating of
. visual space in human parietal cortex. J Neurosci 2003; 23:6209–6214.
in three cortical eye fields of the monkey during an adaptive decision-making
task. J Neurosci 2002; 22:5081–5090. This fMRI study showed that the human PPC dynamically updates the spatial goals
for action in a gaze-centred frame.
32 Pierrot-Deseilligny C, Müri RM, Rivaud-Péchoux S, et al. Cortical control of
spatial memory in humans: the visuo-oculomotor model. Ann Neurol 2002; 54 Van Donkelaar P, Müri RM. Craniotopic updating of visual space across
52:10–19. saccades in the human posterior parietal cortex. Proc R Soc Lond 2002;
269:735–739.
33 Pierrot-Deseilligny C, Rivaud S, Gaymard B, Agid Y. Cortical control of
memory-guided saccades in man. Exp Brain Res 1991; 83:607–617. 55 Merriam EP, Genovese CR, Colby CL. Spatial updating in human parietal
. cortex. Neuron 2003; 39:361–373.
34 Müri RM, Vermersch AI, Rivaud S, et al. Effects of single-pulse transcranial This fMRI study showed that after an eye movement a spatial updating of visual
magnetic stimulation over the prefrontal and posterior parietal cortices during information occurs in the human parietal cortex.
memory-guided saccades in humans. J Neurophysiol 1996; 76:2102–2106.
56 De Souza JFX, Dukelow SP, Gati JS, et al. Eye position signal modulates a
35 Leung HC, Gore JC, Goldman-Rakic PS. Sustained mnemonic response in human parietal pointing region during memory-guided movements. J Neurosci
the middle human frontal gyrus during on-line storage of spatial memoranda. J 2000; 20:5835–5840.
Cogn Neurosci 2002; 14:659–671.
57 Yantis S, Schwarzbach J, Serences JT, et al. Transient neural activity in
36 Sakai K, Rowe JB, Passingham RE. Active maintenance in prefrontal area 46 . human parietal cortex during spatial attention shifts. Nat Neurosci 2002;
creates distractor-resistant memory. Nat Neurosci 2002; 5:479–483.
5:995–1002.
37 Ploner CJ, Gaymard B, Rivaud S, et al. Temporal limits of spatial working This interesting fMRI study used a purely attentional paradigm, in which activation
memory in humans. Eur J Neurosci 1998; 10:794–797. was found in the posterior part of the superior parietal lobule and the anterior part
of the inferior parietal lobule (possibly the supramarginal gyrus).
38 Ploner CJ, Gaymard B, Rivaud-Péchoux S, et al. Lesions affecting the
parahippocampal cortex yield spatial memory deficits in humans. Cereb 58 Perry RJ, Zeki S. The neurology of saccades and covert shifts in spatial
Cortex 2000; 10:1211–1216. attention. Brain 2000; 123:2273–2288.
Cerebral cortex eye movement control Pierrot-Deseilligny et al. 25
59 Corbetta M, Kincade JM, Shulman GL. Neural systems for visual orienting 65 Gaymard B, Rivaud S, Cassarini JF, et al. Effects of anterior cingulate cortex
and their relationships to spatial working memory. J Cogn Neurosci 2002; lesions on ocular saccades in humans. Exp Brain Res 1998; 120:173–183.
14:508–523.
66 Milea D, Lehéricy S, Rivaud-Péchoux S, et al. Antisaccade deficit after
. anterior cingulate cortex resection. NeuroReport 2003; 14:283–287.
60 Mort DJ, Perry RJ, Mannan SK, et al. Differential cortical activation during
. voluntary and reflexive saccades in man. NeuroImage 2003; 18:231–246. The anterior cingulate cortex could also control inhibition in the antisaccade
Activation of the posterior cingulate cortex during reflexive visually guided paradigm.
saccades. 67 Olson CR, Musil SY, Goldberg ME. Single neurons in posterior cingulate
cortex of behaving macaque: eye movement signals. J Neurophysiol 1996;
61 Mort DJ, Malhotra P, Mannan SK, et al. The anatomy of visual neglect. Brain 76:3285–3300.
2003; 126:1986–1997.
68 Berman RA, Colby CL, Genovese CR, et al. Cortical networks subversing
62 Ferraina S, Paré M, Wurtz RH. Comparison of cortico-cortical and cortico- pursuit and saccadic eye movements in humans: an fMRI study. Hum Brain
collicular signals for the generation of saccadic eye movements. J Mapping 1999; 8:209–225.
Neurophysiol 2002; 87:845–858.
69 Tanabe J, Tregellas J, Miller D, et al. Brain activation during smooth-pursuit
. eye movements. NeuroImage 2002; 17: 1315-1324.
63 Gaymard B, Lynch J, Ploner CJ, et al. The parieto-collicular pathway:
. anatomical location and contribution to saccade generation. Eur J Neurosci The authors describe activation of the posterior cingulate cortex during pursuit eye
2003; 17:1518–1526. movements.
This anatomical and lesional study confirmed that the PEF, via its direct projection 70 Hopfinger JB, Buonocore MH, Mangun GR. The neural mechanisms of top-
to the superior colliculus passing through the posterior part of the internal capsule, down attentional control. Nat Neurosci 2000; 3:284–291.
is involved in reflexive saccade generation but not in intentional saccade
generation. 71 Small DM, Gitelman DR, Gregory MD, et al. The posterior cingulate and
. medial prefrontal cortex mediate the anticipatory allocation of spatial attention.
64 Paus T, Petrides M, Evans AC, Meyer E. Role of the human anterior cingulate NeuroImage 2003; 633–641.
cortex in the control of oculomotor, manual, and speech responses: a This important fMRI study suggested that the posterior cingulate cortex is involved
positron emission tomography study. J Neurophysiol 1993; 70:453–469. in the preparation of on-going attentional mechanisms via a motivation process.